Introduction

Successful recognition is supported by a large network of brain regions including medial temporal, prefrontal and parietal areas. Activity in the ventral striatum (VS) is also associated with retrieval success, i.e. VS activity is higher for correctly recognized old items than for correctly rejected new items [1]–[4]. However, the functional significance of ventral striatal activity during recognition has so far received little scientific attention. This area has usually been studied as a central part of the reward circuit, which is involved in reinforcement learning and motivational behaviour [5]. In addition, the VS is associated with the processing of salience and novelty [6], [7].

Based on the prominent role of the VS in the reward circuit, it has been speculated that its retrieval success activity reflects that humans value hits more than correct rejections in a standard recognition memory test [1]. Only recently has a study directly examined the role of the VS in recognition memory [8]. The authors investigated whether VS activity signals successful retrieval triggered by hippocampal and thalamic regions (‘retrieval-dependent account’) or whether VS activity reflects a subjective preference for detecting a previously studied item (‘goal-dependent account’). After studying word lists, subjects were cued whether hits or correct rejections were rewarded in the subsequent recognition test-phase in order to manipulate the motivational status of ‘old’- and ‘new’-responses. In both conditions, responses concordant with the incentive manipulation led to increased striatal activity, i.e. ‘new’-responses were associated with striatal activity when correct rejections were externally incentivized and ‘old’-responses were associated with VS activity when hits were rewarded [8].

This pattern of results implies that striatal activity during recognition is the result of an active evaluation process rather than an automatic consequence of memory reactivation. Thus, it corroborates the goal-dependent account. Especially the unusual activity elicited by ‘new’-responses (when rewarding correct rejections) implicates that the striatal response during recognition is context-sensitive and modulated by the adaptive significance of “oldness” or “newness” to the current goals [4]. This conclusion is supported by enhanced striatal activity for novel items observed in other, non-recognition memory contexts, since such a novelty response would be not consistent with an automatic striatal response to perceived oldness [6], [9]. In summary, the VS seems to assign a subjective value to the degree of familiarity of an item that depends on the current behavioural goals [4].

The goal-dependent hypothesis suggests that also other deviations from standard recognition tests that affect the subjective value of specific response types should modulate the VS activity pattern. In the current study, we explored VS activity in an unusually difficult recognition test that was characterized by very low levels of confidence and accuracy. Based on the human uncertainty aversion [10], [11], the subjective value of all high confident decisions is expected to be higher than usual in such a recognition context, i.e. also rejecting items with high certainty is evaluated as concordant with the current goals. Accordingly, one would hypothesize that VS activity in such a recognition test is not only correlated with retrieval success, but in addition with mnestic confidence not only for ‘old’- but also and ‘new’-responses. On the other hand, when mnestic confidence was previously investigated using standard recognition tests with relatively high certainty, activity in the ventral, reward-associated part of the striatum was not reported by the vast majority of studies – with the exception of one study that observed a small cluster of superthreshold voxels [12]–[18]. Therefore, the VS seems not to be an obligatory node in the confidence network for recognition tasks with the usual high rate of high confidence responses. Moreover, these studies - with one exception - analysed only activity associated with correct ‘old’-responses, i.e. hits, of varying confidence [17]. For this reason, their findings cannot be generalized to the neural correlates of confidence for ‘new’- and incorrect responses. In summary, the present study aimed at exploring the hypothesis that high uncertainty during recognition leads - in contrast to standard paradigms - to VS activity correlated with mnestic confidence for both ‘old’- and ‘new’-responses. To validate that VS activity is, as hypothesized, related to the subjective value of different retrieval outcomes, participants rated in an accompanying behavioural experiment the pleasantness of each recognition response. This procedure avoids reverse inference from VS activity to the subjective value of the various confidence levels [19].

The unusually high false alarm and miss rates in the present recognition paradigm provided the opportunity to test, as a subordinate hypothesis, whether the correlation of retrieval success with VS activity is influenced by the correctness of ‘old’- and ‘new’-decisions. According to the goal-dependent account, the subjective perception of oldness (‘perceived oldness’) [20] should correlate with VS activity independent of the factual status of an item, i.e. hits or false alarm [4].

Materials and Methods

Results

Behavioural Results

Memory performance.

For Experiment 1, the analysis of the behavioural data revealed that neither correctness nor confidence during recognition were influenced by the encoding manipulation(accuracy F(1,18) = 0.3, n.s.; confidence F(1.9,35.9) = 1.4, n.s.) [22]. Therefore, memory performance for this group was pooled across encoding conditions. For both, Experiment 1 and 2, recognition performance was very low (see Table 1). But, the corrected hit (hit – false alarms of the same confidence level) and corrected rejection (correct rejections – misses of the same confidence level) rates were above chance (with the exception of low confidence hits, experiment 1: t(18) = 1.1, n.s., experiment 2: t(18) = 1.9, n.s.). High confidence responses were significantly less frequent than the other two confidence ranks (experiment 1: F(2,36; Greenhouse-Geisser (GG) 1.5,26,8) = 12.4, p<0.05, experiment 2: F(2,36; GG 1.4,25.9) = 17.4, p<0.05, Bonferroni pairwise comparisons p<0.05). Targets and lures were experienced as highly similar, indicated by a d-prime of 0.61 and 0.62 (response criterion 0.14 and 0.18, for Experiment 1 and Experiment 2 respectively).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 1. Descriptive statistics of the behavioural data (Proportion of all trials, standard deviation in parentheses, confidence ratings: 1: high confidence old, 6: high confidence new).

https://doi.org/10.1371/journal.pone.0054324.t001

Pleasantness ratings.

The mean pleasantness ratings for different confidence levels are plotted in Figure 1A. A repeated measure ANOVA with the factors ‘old/new-response’ and ‘confidence’ revealed significant main and interaction effects (main effect old/new: F(1,18) = 10.49, p = 0.004; main effect confidence: F(2,36; GG 1.29,23.3) = 62.17, p<0.001; interaction old/new x confidence: F(2,36; GG 1.4, 25.9) = 7.54, p = 0.001). When asked for the criteria for the pleasantness ratings at the end of the experiment, 14 out of 19 participants reported that pleasantness referred to subjective confidence in a given trial. For most of them (n = 9), perceived oldness was a second, subordinated criterion. In contrast, 2 participants reported that they judged old-responses more pleasant than new responses, irrespective of confidence. Two participants were satisfied when their classification matched their feeling about an item. One participant could not provide a precise rule for his pleasantness ratings.

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Figure 1. Activity in the ventral striatum (experiment 1) and pleasantness ratings (experiment 2).

A: Pleasantness ratings (mean±SD) for all confidence levels (1 = high confidence old, 6 = high confidence new), irrespective of correctness. B: Parameter estimates of the third complementary analysis (mean±SEM, in arbitrary units) for all confidence levels (1 = high confidence old, 6 = high confidence new), irrespective of correctness in the peak voxels of the primary conjunction analysis at xyz = [−8 10 −4] and [6 8 −4]). For details of the analyses see the main text.

https://doi.org/10.1371/journal.pone.0054324.g001

Functional Results

The primary analysis revealed that activity correlated with confidence in areas of the ‘confidence-network’: the left angular gyrus, bilateral posterior and anterior cingulate cortices, cunei, inferior frontal gyri as well as hippocampi [17]. Crucially, in the current study, this ‘confidence-network’ was extended to include the bilateral VS (left VS: peak voxel coordinates: xyz = [−8 10 −4], Z-value of peak voxel = 5.43, p<0.001 adjusted for small volume correction (svc.); right VS: peak voxel xyz = [6 8 −4], Z = 5.14, p<0.001 svc; Figure 2).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Figure 2. Ventral striatal activity related to perceived oldness (p.o.) and confidence (c.).

Red clusters represent the results of the conjunction analysis; yellow clusters represent increased striatal activity due to increasing confidence exclusively masked by perceived oldness. The bars represent the parameter estimates (β; mean±SEM, in arbitrary units) of the corresponding parametric regressors (see text for details of the analysis). For visualization purposes, a threshold of p<0.001 uncorrected was applied.

https://doi.org/10.1371/journal.pone.0054324.g002

The first complementary analysis confirmed that activity correlated with confidence for both ‘old’- and ‘new’-decisions (left VS peak voxel xyz = [−12 16 −4], Z = 3.36, p = 0.006 svc.; right VS peak voxels xyz = [8 8 −4], Z = 3.26 p = 0.008 svc.; xyz = [12 10 −10], Z = 3.23 p = 0.009 svc.; Figure 3 top). Moreover, this correlation between confidence and VS activity was evident independent of the correctness of the response, as revealed by the second complementary analysis (left VS peak xyz = [−12 16 −4], Z = 3.62, p = 0.004 svc.; right VS peak voxel xyz = [−12 16 −4], Z = 3.82, p = 0.002, svc.; Figure 3 bottom).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Figure 3. Top: Ventral striatal activity related to confidence for perceived ‚old‘- and ‚new’-responses, i.e. hits and false alarms, correct rejections and misses; Bottom: Ventral striatal activity related to confidence for correct and incorrect responses, i.e. hits and correct rejections, false alarms and misses.

The bars represent the parameter estimates (β; mean±SEM, in arbitrary units) of the corresponding parametric regressors in the peak voxel named above the bars. For visualization purposes, a threshold of p<0.001 uncorrected was applied.

https://doi.org/10.1371/journal.pone.0054324.g003

Bilateral VS activity was also correlated with perceived oldness, i.e. activity was greater during ‘old’- than ‘new’-decisions (same peak voxels as in the ‘confidence’ analysis; left VS: peak voxel xyz = [−8 10 −4]; Z = 5.03, p<0.001, svc.; right VS: peak voxel xyz = [6 8 −4]; Z = 3.92, p = 0.001, svc.). The second complementary analysis revealed that this enhanced activity for perceived oldness was independent of the factual status of an item, i.e. VS activity was greater for hits than correct rejections and for false alarms than misses (left VS: xyz = [−8 10 −4], Z = 4.15, p<0.001 svc; right VS: xyz = [10 14 −4], Z = 2.88, p<0.025 svc).

The conjunction analysis of confidence and perceived oldness revealed that activity in overlapping areas of the VS correlate with both confidence and perceived oldness (left VS: peak voxel xyz = [−8 10 −4], Z = 5.03, p<0.001, svc.; right VS: peak voxel xyz = [6 8 −4], Z = 3.92, p = 0.001, svc.; Figure 2). Exclusive masking revealed that activity in more right ventral and bilateral anterior areas of the VS correlated significantly only with confidence but not with perceived oldness (left anterior VS: peak voxel xyz = [−12 18 −6]; Z = 4.2, p<0.001, svc.; right inferior ventral VS: peak voxel xyz = [10 10 −10], Z = 4.55, p<0.001, svc.; right anterior VS: peak voxel xyz = [12 16 −8], Z = 3.18, p = 0.01, svc.; Figure 2). This descriptive activity difference was corroborated statistically and the differential contrast, i.e. confidence +1 and perceived oldness −1, revealed a cluster in the right ventral VS (peak voxel: xyz = [12 10 −10]; Z = 2.77, p<0.05, svc.). No significant activation was found in the reverse masking and differential contrast analyses.

The results of the third complementary analysis to characterize the relationship between confidence and VS activity are plotted in Figure 3B and suggest a linear response function. A perceived oldness/newness x confidence ANOVA revealed for the right and left VS significant effects of perceived oldness/newness and confidence (right VS: old/new F(1,17) = 7.47, p = 0.01, confidence F(2,34; 1.63,27.72) = 13.11, p<0.001; left VS: old/new F(1,17) = 16.05, p<0.001, confidence F(2,34; GG 1.61,27.38) = 9.49, p<0.001). This ANOVA confirmed therefore the results of the primary analysis.

Discussion

VS activity correlated in the current unusually difficult recognition test not only with retrieval success, but also with confidence. Moreover, consistent with the well described uncertainty aversion [10], [11], participants indicted in the behavioural experiment that they were more satisfied by higher confidence in addition to perceived oldness, which parallels the VS activity pattern. In contrast, the vast majority of previous item-memory studies on the neural correlates of recognition confidence did not observe VS activity above the statistical threshold [12]–[18]. Only two difficult source memory studies reported larger clusters of VS activity to be associated with confidence [23], [24]. This across study pattern implies that the VS is not an obligatory node of the ‘confidence’-network, as e.g. parietal areas, but that its correlation with confidence might be a function of task difficulty. Therefore, it is plausible to attribute its correlation with confidence in the present study to the unusual task difficulty that resulted in high subjective values of all high confident retrieval outcomes. The observed context sensitivity of the striatal signal parallels the findings of Han and colleagues who increased the subjective value of correct rejections by external incentives. Taken together, the results are therefore in line with the hypothesis that VS activity during recognition is not an automatic result of memory reactivation, but codes the subjective value of different response types that is modulated by context [4], [8].

In the decision making literature, the high subjective value of certain information in an uncertain environment was recently illustrated by the willingness to pay for information [25]. The resulting increase in decision confidence correlated with VS activity and even certain information about upcoming punishments activated the VS [26]. An increase in striatal activity without feedback has also been reported during working memory and category learning, which supports the notion that the satisfaction of internal goals and incentives can drive striatal activity [27], [28]. In the category learning study, VS activity was, similar to the present data, correlated with confidence and, moreover, also with the prediction errors on confidence [27]. In the present recognition test, subjects either from the very beginning or rapidly develop the expectation that they will have only low confidence in their judgements. Therefore, the VS activity could represent, in addition to the subjective values of retrieval outcomes, positive prediction errors on the rare high confidence events.

The VS also plays a role in the detection of non-rewarding deviant and salient stimuli [7], [29]–[32]. However, the resulting alternative interpretation of the VS activity, i.e. that it may be related to the salience of the relatively few high confidence items in the overall low confidence context, seems unlikely given that the pleasantness ratings of the subjects parallel striatal activity.

Activity in parts of the VS was not only related to confidence but also to perceived oldness, i.e. the well documented retrieval success effect. Moreover, participants reported post experimentally that both, confidence and perceived oldness, satisfied their goals where confidence was the dominant cause for pleasantness. Together, this might imply that even in a context of high uncertainty the subjective value of detecting targets is higher than of detecting lures, i.e. that the subjective value of a given retrieval outcome is a function of both perceived oldness and confidence. Alternatively, the correlation of VS activity and pleasantness with both confidence and perceived oldness could also indicate two independent underlying processes. Recently, an elaborate review hypothesized three, non-mutually exclusive processes that potentially account for the striatal activity associated with retrieval success [4]. It will be discussed in the following whether the three process would also account equally well for the correlation with confidence, in particular for perceived new items.

According to the ‘Retrieval as Adaptive Encoding’-hypothesis, the VS modulates the re-encoding of items dependent on their subjective value, i.e. their behavioural relevance and the likelihood of their future utility [4]. The authors argue that the retrieval of an item in a given context signals a higher utility of that item, i.e. this item might be useful in the same context again. This re-encoding interpretation is supported by the involvement of the VS in encoding information beyond that associated with reward [33]–[35]. Moreover, it is known from the ‘testing effect’-literature that retrieval-attempts drive successful (re)-encoding, in particular for ‘old’-responses, which is amplified by confidence [36]. In agreement with this interpretation, a recent model suggests that dopaminergic neurotransmission in the ventral tegmental-hippocampal loop might underlie the re-encoding during retrieval [37]. The adaptive encoding hypothesis seems able to explain the confidence dependent activity for perceived old items in the present study. Moreover, re-encoding also of high confident rejected items in an uncertain context is consistent with this view since cognitive control determines which retrieval outcome is of high utility in a given situation, i.e. all high confidence items have a high utility in an uncertain context.

The ‘Reinforcement Learning and Adaptation of Cognitive Control at Retrieval’-hypothesis proposes that striatal activity is related to the evaluation of the employed retrieval strategies [4]. The VS codes expectations about the value of a retrieval strategy and computes a negative prediction error when a given stagey is ineffective, i.e. does not result in the desired retrieval outcome. This hypothesis is then also consistent with the correlation of VS activity with confidence for ‘old’- and ‘new’-responses in the present study. Since high confident rejections also have a high subjective value in this context, retrieval strategies that led to such an outcome would be reinforced by a positive prediction error. However, note that this positive prediction error over retrieval strategies differs conceptually from the prediction error over rare, pleasant, high confident decisions that were discussed earlier together with the category learning study [27].

The ‘Adaptive Gating of Working Memory to Control Retrieval’ hypothesis states that the striatum - though not necessarily ventral striatum - might be involved in selecting which representations to admit into working memory in order to increase the likelihood of a successful retrieval outcome and/or successful performance on the task overall. Thus, assuming that confidence reflects the strength of the decision that an item is old or new, then more confident decisions would have higher adaptive value for making a response. In other words, high confidence old or new are more likely to yield correct responses. Thus, striatal activation would track confidence in the task accordingly.

In conclusion, the three hypotheses account equally well for the correlation of VS activity with perceived oldness and with confidence, but only in a context which increases the subjective value of all types of high confidence retrieval outcomes. Therefore, it cannot be decided whether the three hypothesized processes contribute differently to the correlation of VS activity with perceived oldness and confidence. As a consequence, it cannot be inferred based on the hypotheses whether distinct processes in the VS might be the basis for the observed correlations with perceived oldness and confidence.

However, in reference to the question of whether the same or different processes in the VS correlate with confidence and perceived oldness, the exclusive masking descriptively showed a larger cluster in the bilateral VS to be correlated with confidence, a finding that was statistically confirmed for the right VS (Figure 2). This activity pattern was somehow paralleled by the post experimental reports of subjects, where most indicated that confidence was dominant for their pleasantness ratings followed by perceived oldness. Therefore, a potential contribution of different processes to the signal correlated with perceived oldness and confidence could be paralleled by a functional subdivision of the VS during recognition, especially since such a specialization has been suggested based on connectivity patterns [38].

The observed VS activity increase for retrieval success replicates many previous findings. It was hypothesized that this activity reflects the higher subjective value of hits than correct rejections in a standard recognition memory test, which was confirmed by the old/new effect in the pleasantness ratings of the present study [1], [8]. To test the subordinate hypothesis, it was moreover shown in the present experiment that the retrieval success effect in the VS does not differ significantly for true and false memories. On the contrary, using Deese–Roediger McDermott-paradigms, it has been shown that activity in other areas correlates with the factual memory status, i.e. is higher for hits than false alarms [39]. For example, greater activity for hits in the parahippocampus was explained by the reactivation of perceptual, or other encoding-related information, that is missing for false alarms. Based on these findings, the insensitivity of the VS to the factual status of a probe item in the current study provides evidence for the previous conclusion that VS activity is not triggered automatically by the outcome of retrieval, i.e. does not reflect the ‘retrieval-dependent’-account [8]. Perceived oldness during recognition has received much less attention than the retrieval success effect, presumably because of the high number of false alarms required for this type of analysis [20], [40]. Therefore, it cannot be determined based on the literature whether the correlation of VS activity with perceived oldness is a result of the unusually high rate of incorrect responses in the current paradigm or a general feature thereof.

Acknowledgments

We would like to thank Jan Peters and Eszter D. Schoell for helpful comments. In addition, for providing the Harvard-Oxford Atlas as implemented in FSL, we are very grateful to David Kennedy, Christian Haselgrove, Bruce Fischl, Janis Breeze, Jean Frazier, Larry Seidman and Jill Goldstein.